New Anatomical Information of the Wukongopterid Kunpengopterus Sinensis Wang Et Al., 2010 Based on a New Specimen

New anatomical information of the wukongopterid Kunpengopterus sinensis Wang et al., 2010 based on a new specimen

Xin Cheng1,2, Shunxing Jiang1, Xiaolin Wang1,3 and Alexander W.A. Kellner2

1 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China 2 Laboratory of Systematics and Taphonomy of Fossil Vertebrates, Department of Geology and Paleontology, National Museum/UFRJ, Rio de Janeiro, Brazil 3 University of Chinese Academy of Sciences, Beijing, China

ABSTRACT The Wukongopteridae compose a non-pterodactyloid clade of pterosaurs that are the most abundant flying reptiles in the deposits of the Middle-Late Jurassic Yanliao Biota. Until now, five species of three genera and two additional unnamed specimens have been described. Here we report on a new material, IVPP V 23674, that can be referred to the wukongopterid Kunpengopterus sinensis due to several features such as a comparably short nasoantorbital fenestra, the dorsally rising posterodorsal margin of the ischium, and the very short first pedal phalanx of digit V relative to metatarsal IV. IVPP V 23674 provides the first view of a wukongopterid palate, which differs from all other pterosaurs by having a very large postpalatine fenestra and laterally compressed choanae, indicating that the evolution of the pterosaur palate was more complex than previously thought. Sesamoid bones at the dorsal side of manual unguals are present and are reported for the first time in a wukongopterid suggesting an arboreal life-style for these pterosaurs.

Subjects Paleontology Submitted 6 July 2017 Keywords Kunpengopterus sinensis, Wukongopteridae, Pterosauria, Yanliao Biota, Late Jurassic, Accepted 7 November 2017 China Published 1 December 2017 Corresponding author Xiaolin Wang, INTRODUCTION [email protected] Pterosaurs are the first vertebrates to achieve powered flight. These flying reptiles developed Academic editor Hans-Dieter Sues a comparatively fragile skeleton that resulted in a generally limited preservation potential Additional Information and (e.g., Wellnhofer, 1991; Kellner, 1994). As a consequence, except for three so far monotaxic Declarations can be found on bonebeds (Chiappe et al., 2000; Wang et al., 2014a; Manzig et al., 2014), most species are page 15 represented only by one or two specimens (e.g., Wang et al., 2007; Wang et al., 2014b; Jiang DOI 10.7717/peerj.4102 & Wang, 2011; Cheng et al., 2015). Copyright In the last ten years, important new pterosaur discoveries have been made in several 2017 Cheng et al. regions of China, mostly coming from the Late Jurassic Tiaojishan Formation and the Early Distributed under Cretaceous Jehol Group (e.g., Wang et al., 2009; Wang et al., 2012; Wang et al., 2014b; Wang Creative Commons CC-BY 4.0 et al., 2015; Lü et al., 2010; Lü et al., 2011a; Lü et al., 2011b; Cheng et al., 2012; Cheng et al., OPEN ACCESS 2015; Cheng et al., 2017; Jiang et al., 2014; Jiang et al., 2016; Rodrigues et al., 2015). Among

How to cite this article Cheng et al. (2017), New anatomical information of the wukongopterid Kunpengopterus sinensis Wang et al., 2010 based on a new specimen. PeerJ 5:e4102; DOI 10.7717/peerj.4102 the most exciting discoveries done recently are the Wukongopteridae, whose members combine characters from both, basal non-pterodactyloids and derived pterodactyloids (e.g., Wang et al., 2009; Lü et al., 2010; Cheng et al., 2016). So far, six specimens of this non-pterodactyloid clade have been described and referred to three genera and five species (Wang et al., 2009; Wang et al., 2010; Lü et al., 2010; Lü et al., 2011a). In addition, there is Changchengopterus pani, known from two individuals (Lü, 2009; Zhou & Schoch, 2011), that is regarded as a potential wukongopterid (Wang et al., 2009; Cheng et al., 2017), and another three undetermined specimens (Lü et al., 2011b; Cheng et al., 2016; Cheng et al., 2017). Furthermore, there are several undescribed fossils scattered throughout many collections in China that most certainly belong to this clade. Here we report on a second specimen (IVPP V 23674) of Kunpengopterus sinensis that provides supplementary anatomical information for this genus, including details of the foot and caudal vertebrae, allowing us to revise the diagnosis of this species. This material also makes it possible to describe, for the first time, the palate of a wukongopterid that reveals several significant differences from other pterosaurs.

MATERIALS AND METHODS IVPP V 23674 consists of a nearly complete skeleton with the skull exposed in right lateral view. It was recovered from the Yanliao deposits near Daxishan (Linglongta, Jianchang, Liaoning Province, China). The specimen was collected by a local resident and is presently housed at the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences (IVPP/CAS). It arrived at the IVPP divided into several parts that were put together using epoxy glue and was prepared mechanically by steel needle and pneumatic micro tools under a microscope. Photographs were taken using camera Nikon D3X and combined into a fully focused image using Helicon Focus 6.7.1 software.

RESULTS Systematic paleontology

Pterosauria Kaup, 1834 Wukongopteridae Wang et al., 2009 Kunpengopterus Wang et al., 2010 Kunpengopterus sinensis Wang et al., 2010

Holotype IVPP V 16047, an almost complete skeleton with the complete skull and lower jaw housed at the Institute of Vertebrate Paleontology and Paleoanthropology (Chinese Academy of Sciences), Beijing, China. Referred specimen A nearly complete skeleton including the skull and lower jaw (IVPP V 23674), housed at the IVPP (Fig. 1).

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 2/20 Figure 1 The complete skeleton of Kunpengopterus sinensis (IVPP V 23674). (A) Photo and (B) line drawing with missing portions of the skeleton were preserved as impression in dark grey. Scale bars: 50 mm. Abbreviations: at, atlas; ax, axis; cdv, caudal vertebra; cor, coracoid; cv3–7, third to seventh cervical vertebra; dca, distal carpal series; fe, femur; fo, foramen; hu, humerus; hy, hyoid bone; il, ilium; is, ischium; l, left; mcIV, metacarpal IV; pca, proximal carpal series; ph1–4d4, first to fourth phalange of manual digit IV; plca, proximal lateral carpal; ppu, prepubis; ptd, pteroid; r, right; pu, pubis; ra, radius; sca, scapula; st, sternum; sv, sacral vertebra; ti, tibia; ul, ulna. Full-size DOI: 10.7717/peerj.4102/fig-1

Emended diagnosis Wukongopterid pterosaur with the following combination of characters that distinguishes it from other members of this clade (autapomorphies are marked with an asterisk): posterior region of the skull rounded*; absence of premaxillary crest; nasoantorbital fenestra around 40% the skull length*; maxillary process of the jugal thin and relatively short*; lacrimal process of the jugal thick; presence of a soft tissue crest above the frontal; posterodorsal margin of ischium rising dorsally; proximal end of prepubis very short and wide*; first pedal phalanx of digit V short, less than 70% of metatarsal IV*; curved second pedal phalanx of the fifth toe with an angle between the proximal and distal segments about 145◦*; proximal segment of the second pedal phalanx of the fifth toe about 30% length of the distal segment, shorter than in other wukongopterids* (modified from Wang et al., 2010).

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 3/20 Figure 2 Details of the skull of Kunpengopterus sinensis (IVPP V 23674). (A) Close up of the right lateral view. (B) Line drawing, with missing parts and regions covered by other skeletal elements in dark grey. Scale bars: 50 mm. Abbreviations: ch, choana; ec, ectopterygoid; f, frontal; fona, foramen nasale; j, jugal; l, left; la, lacrimal; m, maxilla; n, nasal; naof, nasoantorbital fenestra; pl, palatine; pm, premaxilla; pplf, postpalatine fenestra; prn, process of nasal; pty, pterygoid; ptyf, pterygoid fenestra; q, quadrate; qj, quadratojugal; scl, sclerotic ring; sstf, secondary subtemporal fenestra; te, teeth; v, vomer; ?, uncertain. Full-size DOI: 10.7717/peerj.4102/fig-2

Locality and horizon Daxishan, Linglongta, Jianchang, Liaoning, China. Tiaojishan Formation (= Daohugou Bed) Late Jurassic (Zhou, Jin & Wang, 2010; Cheng, 2013; Wang et al., 2014c; Sullivan et al., 2014). Description and comparison IVPP V 23674 is preserved in a grey-white slab of shale associated with many conchostracans that indicate a freshwater lacustrine environment (Fig. 1). It is composed of a nearly complete skeleton only lacking the tip of the left wing and most of both femora. The skull and lower jaws are complete but disarticulated, with the posterior portion compacted and covered by other bones. Most of the remaining portion of the skeleton is present, with elements closely associated or in articulation (e.g., the right wing, tibiae and feet). The close association of the bones indicates that they represent one individual. As in the holotype, the skull is elongated and lacks a premaxillary crest (Fig. 2), differing from Darwinopterus (Wang et al., 2010; Lü et al., 2010; Lü et al., 2011a) and IVPP

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 4/20 V 17959 (Cheng et al., 2016). The length of the nasoantorbital fenestra relative to the skull length is the shortest among all wukongopterids (∼40.1%, Table 1; Cheng et al., 2017). Unfortunately, this region in the holotype (IVPP V16047) is not complete, but based on the preserved portion, the maximum length of this opening relative to the skull length is estimated as being very similar to IVPP V 23674 (∼41%, Table 1). The premaxilla and maxilla are fused, and no suture is visible (Fig. 2). The posterior end of the premaxillae separates the anterior end of the frontals. On the dorsal margin of the premaxillae, a low bony ridge is present that does not form a premaxillary crest, differing in this respect from Darwinopterus and other wukongopterid specimens (Wang et al., 2010; Lü et al., 2010; Lü et al., 2011a; Cheng et al., 2016; Cheng et al., 2017). As in the holotype, the maxilla process of the jugal is thin and short (Fig. 2). It occupies about 25% the length of the ventral margin of the nasoantorbital fenestra, being much shorter than in Darwinopterus linglongtaensis where this ratio is about 50%. The lacrimal process of the jugal is wide and differs from the thinner condition of this bone in Darwinopterus linglongtaensis and IVPP V 17959 (Wang et al., 2010; Cheng et al., 2016). The nasal bears a thin anteroventrally inclined process (Figs. 2 and 3), which is like the one of Darwinopterus (Wang et al., 2010; Lü et al., 2010; Lü et al., 2011a) and different from the subvertical process present in IVPP V 17959 (Cheng et al., 2016). The holotype of Kunpengopterus sinensis (IVPP V16047) was originally described as having a broad nasal process, with an elliptical foramen at the middle portion (Wang et al., 2010). However, based on our reexamination of this specimen, the ‘‘broad’’ condition is the result of the overlap of the nasal processes from both sides. There is a foramen positioned at the base of this process. The posterior region of the skull suffered from severe compression. Several elements have been displaced from their original anatomical position and are broken, making their identification difficult. The shape of the orbit cannot be established. There are about ten small bony plates that made part of the sclerotic ring. An elongated bone displaced ventrally is interpreted as the lacrimal, showing a large opening, similar to the one reported in IVPP V 17959 (Cheng et al., 2016). The quadrate is also displaced and exposed in medial view (Fig. 2). It shows the ventral portion expanded, has a developed medial flange, and shows a deep medial fossa above the articulation (Fig. 4E). The palate is exposed in dorsal view through the nasoantorbital fenestra with the anterior and posterior portions embedded in the matrix (Figs. 2 and 5). The choanae are elongated (length of the right one - 18.9 mm) and laterally compressed, divided by a thin vomer. The postpalatine fenestrae are extremely elongated, more than in any non-pterodactyloid. They are pear-shaped with the maximum length around 19 mm (preserved length: 18.8 mm) and maximum estimated width around 3.5 mm (preserved width: 3.4 mm). Each is followed by a secondary subtemporal fenestra, which has an overall quadrangular shape (Figs. 2 and 5). Only the anterior margin of the left subtemporal fenestra, made by a lateral extension of the pterygoid, is observed. There is a tiny opening between the pterygoids that appears to be the pterygoid fenestra. No clear distinction between the ventral part of the maxillae and the palatines is perceptible. The ectopterygoids are compressed and have a posterior ascending process.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 5/20 Table 1 Measurements (in mm) of two specimens of Kunpengopterus sinensis: IVPP V 23674 (referred specimen) and IVPP V 16047 (holotype).

Bones IVPP V 23674 IVPP V 16047 IVPP V 23674 / IVPP V 16047 sq-pm ∼120.0 106.9 ∼112% ros 43.8 ∼40.5 ∼108% naof 48.8 max 43.9a min 111% man.sys 27.9 – sca 33.0(l) ∼28.8(r) ∼115% cor 28.9(r) 28.3(l) ∼23.8(l) ∼119% hu 42.8(r) 39.6a(r) 108% ul 66.2(r) 64.5(l) ∼59.2(l) ∼109% mcIV 26.9(r) 27.6(l) ∼23.0(l) ∼120% ph1d4 52.8(r) 52.8(l) ∼54.2(r) ∼97% ph2d4 58.6(r) 58.5(l) 58.0(r) 101% ph3d4 59.1(r) 59.0(l) 59.2(r) 100% ph4d4 53.9(r) ∼110% ∼48.8(l) ti 56.1(r) 103% 54.5(l) mt1 22.6(r) 22.4a(r) 101% 22.9(l) 21.6a(l) 106% mt2 23.1(r) 23.2a(r) 100% 23.2(l) 22.1a(l) 105% mt3 21.6(r) 21.8(r) 99% 20.8(l) 20.7(l) 100% mt4 18.8(r) 17.9(r) 104% 17.9(l) pph1d5 11.8(r) 11.2(r) 106% 12.2(l) this paper (Wang et al., 2010) and this paper

Notes. aNew values based on the reexamination of IVPP V 16047. Abbreviations: cor, coracoid; hu, humerus; l, left; man.sys, mandibular symphysis; max, maximum; mcIV, metacarpal IV; min, minimum; mt1–4, metatarsal I–IV; naof, nasoantorbital; ph1–4d4, first to fourth phalanx of manual digit IV; pm, premaxilla; pph1d5, first phalanx of pedal digit V; r, right; ros, rostrum; sca, scapula; sq, squamsal; ti, tibia; ul, ulna. They form the posterior margin of the postpalatine fenestrae. The pterygoids show a complex morphology and participate in every fenestra of the palate. The lower jaw is exposed in ventral view (Fig. 1). Its exact length cannot be determined since the posterior end of the mandibular ramus from both sides is covered by other

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 6/20 Figure 3 Comparison between the nasal processes of both specimens of Kunpengopterus sinensis; IVPP V 23674 (referred specimen) and IVPP V 16047 (holotype). Close up (A) and line drawing (B) of the nasal processes of IVPP V 23674. Close up (C) and line drawing (D) of the nasal processes of IVPP V 16047. Scale bars: 10 mm. Abbreviations: fona, foramen nasale; l, left; pm, premaxilla; prn, process of nasal; r, right. Full-size DOI: 10.7717/peerj.4102/fig-3

elements of the skeleton. The dentaries are fused forming an elongated mandibular symphysis (Table 1). The preserved angle between both mandibular rami is about 14◦. This new specimen has the dentition better preserved than that of the holotype. Teeth are cone-shaped, with at least fifteen upper and eleven lower teeth. Of these, seven are located on the mandibular symphysis. The last preserved upper tooth is positioned nearly underneath the middle portion of the nasoantorbital fenestra. The interalveolar space of the upper teeth becomes larger posteriorly until the last preserved alveolus that is closer to the preceding one compared to the others. The atlas and axis are not fused (Fig. 4F). The atlas can be observed from the left laterodorsal view and shows the anterior articulation surface more concave than in IVPP V 17959 (Cheng et al., 2016). Only the neural arch from the left side is preserved and is dorsally expanded. The axis bears large postzygapophyses and a developed neural spine. The centrum is biconvex, with the condyle more developed. The lateral side is concave and is perforated by a small foramen.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 7/20 Figure 4 Details of the skeleton of Kunpengopterus sinensis (IVPP V 23674). (A) Close up of the right humerus. (B) Close up of the right coracoid. (C) Close up of the sacral vertebrae, pelvic girdle and prepubis, with the arrow pointing to the anterior tip of the right ilium. (D) Close up of right manual digit I–III, with sesamoid bones preserved at the dorsoposterior region of the unguals. (E) Close up of the quadrate. (F) Close up of the atlas and axis. (G) Close up of the right foot. (H) Close up of the left foot. (I) Close up of the distal end of tail. Scale bars: 10 mm. Abbreviations: ac, acetabulum; at, atlas; ax, axis; co, cotyle; cor, coracoid; dpc, deltopectoral crest; dta, distal tarsal; epi, epiphysis; etp, extensor tendon process; fe, femur; fo, foramen; hu, humerus; il, ilium; is, ischium; l, left; obfo, obturator foramen; mcI–IV, metacarpal I– IV; mfl, medial flange; mfo, medial fossa; mt2, metatarsal II; mt4, metatarsal IV; nc, neural canal; ns, neural spine; ph1d4, first phalanx of manual digit IV; poz, postzygapophysis; pph1d5, first phalanx of pedal digit V; pph2d5, second phalanx of pedal digit V; ppu, prepubis; pu, pubis; q, quadrate; qj, quadratojugal; r, right; ses, sesamoid bone; sv, sacral vertebra; tub, tubercle. The names of palate structures are following Wellnhofer (1978) and Kellner (2013). Full-size DOI: 10.7717/peerj.4102/fig-4

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 8/20 Figure 5 Reconstruction of the partial palate region of Kunpengopterus sinensis (IVPP V 23674) in dorsal view. (A) Close up of the palate. (B) Reconstruction. Scale bars: 10 mm. Abbreviations: ch, choana; ec, ectopterygoid; j, jugal; m, maxilla; pl, palatine; pplf, postpalatine fenestra; pty, pterygoid; ptyf, pterygoid fenestra; sstf, secondary subtemporal fenestra; stf, subtemporal fenestra; v, vomer. The names of palate structures are following Wellnhofer (1978) and Kellner (2013). Full-size DOI: 10.7717/peerj.4102/fig-5

Cervical vertebrae 3 to 7 are elongated compared to other non-pterodactyloids (Fig. 1; Table 2) that is a typical feature of the Wukongopteridae (Wang et al., 2009; Wang et al., 2010; Lü et al., 2010; Lü et al., 2011a; Cheng et al., 2016). A lateral depression can be observed on the centrum of cervical 3 and 6, but it is not sure if it leads to a foramen. Several cervical vertebrae show small cervical ribs. At least 11 dorsal vertebrae, mostly disarticulated, could be identified and do not form a notarium. Some show a foramen on the ventral side of the transverse process. Five sacral vertebrae, all fused, are present with most of the left side broken away (Fig. 4C). The tail shows at least twenty-six articulated caudal vertebrae (Figs. 1, 4I). Except for the last one, all are enclosed by rod-like extensions of the zygapophyses and chevrons, a typical feature of non-pterodactyloids. The sixth preserved caudal vertebra is the longest, and all after this one decrease gradually in size (Table 3). No trace of a tail vane is preserved.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 9/20 Table 2 Measurements of cervical vertebrae of Kunpengopterus sinensis (IVPP V 23674) (in mm).

Cervical vertebrae Length atlas 1.2 axis 6.8 3rd 11.5 4th ∼13.3 5th 13.0 6th 12.1 7th 8.6

Table 3 Measurement of caudal vertebrae of Kunpengopterus sinensis (IVPP V 23674) (in mm). The measurements follow the sequence of the preserved elements. The tail is incomplete and the first caudal vertebrae are not preserved.

Preserved Length Preserved Length Preserved Length vertebrae vertebrae vertebrae 1 – 10 11.54 19 7.14 2 3.15 11 11.26 20 6.46 3 – 12 10.84 21 5.48 4 – 13 10.24 22 4.69 5 11.86 14 9.61 23 3.83 6 12.59 15 9.11 24 3.45 7 12.17 16 8.88 25 2.91 8 12.01 17 8.66 26 0.55 9 11.88 18 7.69 Notes. –, measurement not possible due to preservation. The sternum is exposed in dorsal view and is partially covered by the right scapula, coracoid and humerus (Figs. 1, 4A, 4B). This bone is heart-shaped, being longer (40.4 mm) than wide (28.3 mm). The articular facets for the coracoids are asymmetrical and positioned laterally, with the right one in front of the left. A large and rounded foramen is present posterior to the cristospine. Scapula and coracoid from both sides are preserved, with the former longer than the latter (Table 1). They are fused forming a scapulocoracoid (Fig. 1). The scapula has an elongated and dorsoventrally compressed posterior end. The coracoid bears a well-developed lateral tubercle positioned close to the coracoid process (Fig. 4B), which is also seen in IVPP V 17959 (Cheng et al., 2016). The articulation surface of the coracoid with the sternum is concave and lacks a posterior expansion (Fig. 4B). Both humeri are preserved, with the left one covered by other skeletal elements. The right humerus is exposed in dorsolateral view, has a slightly curved shaft and shows a foramen on the dorsal surface at the level of the distal margin of the deltopectoral crest (Fig. 4A), similar to that of Darwinopterus linglongtaensis (Wang et al., 2010). The deltopectoral crest is placed proximally and expands distally, without a neck or the hatch-shaped condition seen in Rhamphorhynchus (Wellnhofer, 1978; Kellner, 2003). The distal end of the left

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 10/20 humerus is exposed in ventral view and apparently has the epiphysis fused (Fig. 4A). The ulnae and radii are well preserved, with the diameter of the radius smaller but larger than half that of the ulna (Fig. 1). The carpal region of both sides is well preserved, with all elements of the proximal and distal carpal series fused. The right distal carpal series can be observed from distal view and shows a trapezoidal outline, with the posterior portion larger than the anterior one (Fig. 1). The right metacarpal region is complete. Metacarpals I–III are all about the same length and show approximately the same thickness. The pteroid is elongated and slightly curved. Manual digits I–III bear curved and sharp unguals, which are of similar size as the pedal unguals. All show a well-developed lateral groove. A sesamoid bone is present at the dorsal side of each right manual ungual (Fig. 4D). Examining the holotype (IVPP V 16047), sesamoid bones were also found in the same region that have been overlocked in the original description. At the tip of two manual unguals of IVPP V 23674, there is a small dorsally curved extension that appear to be pathologic (Fig. 4D). Both first wing phalanges are exposed in dorsal view and have the extensor tendon process fused (Fig. 4D). The first wing phalanx is slightly bent posteriorly, which is a common feature within the Wukongopteridae (Cheng et al., 2016). The length of the first and fourth wing phalanges are smaller than the second and third (Table 1). The right pelvic girdle is preserved and exposed in lateral view (Fig. 4C). All elements are fused to each other but not to the sacral vertebrae. The preacetabular process of the ilium was broken away. A small obturator foramen can be observed below the acetabulum. The ischium forms a broad ventral narrowing plate with a rising posterodorsal margin. The same configuration is observed in the holotype (IVPP V 16047) and differs from Darwinopterus linglongtaensis (Wang et al., 2010). An unusual and plate-like bone is interpreted as the right prepubis since it is tightly connected to the right pubis. Exposed in dorsal view, this element is wide and slightly concave. The anterior margin is clearly thinner than the posterior one, and the articulation with the opposite prepubis is almost straight. Compared to Darwinopterus and IVPP V 17959, the proximal end of this bone is very short and wide (Wang et al., 2010; Lü et al., 2010; Lü et al., 2011a; Cheng et al., 2016). The hindlimbs are not very well preserved and provide only limited information. The distal end of the fibula is fused with the tibia and a clear suture between these elements is only visible at the proximal part. The proximal tarsal elements are fused to the tibia forming a tibiotarsus (Figs. 4G, 4H). Both feet are well preserved. Metatarsal II is the longest while metatarsal IV the shortest, with metatarsal I and III of similar length (Tables 1 and 4; Figs. 4G, 4H, 6). The pedal digit V bears two elongated phalanges, with the first one about 21.2% the length of the tibia. The second phalanx is curved near the proximal end, with the proximal segment about 30% the length of the distal one. The angle between the proximal and distal segments is about 145◦.

DISCUSSION IVPP V 23674 can be classified in the Wukongopteridae since it shares several characters with the members of this clade, including a confluent nasoantorbital fenestra, comparatively

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 11/20 Table 4 Measurements (in mm) and ratios of wukongopterid feet.

Taxa A B A/B C pph1d5 mt2 mt4 pph1d5/ pph1d5/ mt4/ Reference length length length mt2 mt4 mt2 Kunpengopterus sinensis 2.6 8.8 0.30 145◦ 11.2 23.2 17.9 0.48 0.63 0.77 Wang et al., 2010 (IVPP V 16047, holotype) and this paper Wukongopterus lii 6.6 9.0 0.73 71◦ 13.7 18.1 15.0 0.77 0.91 0.83 Wang et al., 2009 and this paper Darwinopterus linglongtaensis 4.5 9.9 0.45 124◦ 12.1 16.8 14.2 0.72 0.85 0.85 Wang et al., 2010 and this paper IVPP V 23674 3.0 10.2 0.29 147◦ 11.8 23.1 18.8 0.51 0.63 0.81 this paper IVPP V 18043 a7.7 a9.7 0.79 a137◦ 18.5 21.0 16.0 0.88 1.16 0.76 Lü et al., 2011b (wukongopterid with eggs) and this paper Darwinopterus robustodens 5.3 11.0 0.48 136◦ 18.1 22.4 18.5 0.81 0.98 0.83 Cheng et al., 2017 and this paper

Notes. ameasurement based on picture. Abbreviations: A, length of proximal segment of second phalanx of pedal digit V; B, length of distal segment of second phalanx of pedal digit V; C, angle between proximal and distal segment of second phalanx of pedal digit V; mt2, metatarsal II; mt4, metatarsal IV; pph1d5, first phalanx of pedal digit V. elongated cervical vertebrae, reduced cervical ribs, and an elongated metacarpal IV (e.g., Wang et al., 2010; Cheng et al., 2017). Wang et al. (2010) also considered the first phalanx of manual digit IV shorter than the fourth as a diagnostic character of this clade, but IVPP V 23674 and at least another two unpublished wukongopterid specimens bear a longer first phalanx of manual digit IV compared to the fourth. This new specimen (IVPP V 23674) is referred to as Kunpengopterus sinensis based on the following features: comparatively short nasoantorbital fenestra relative to the length of the skull, relatively short and thin maxillary process of the jugal, posterodorsal margin of ischium rising dorsally, first pedal phalanx of digit V less than 70% length of metatarsal IV, and second pedal phalanx of the fifth toe curved at an angle of about 145◦, with the proximal segment about 30% the length of the distal one. IVPP V 23674 also differs from Darwinopterus by the absence of a premaxillary crest and a comparably reduced preacetabular portion of the ilium. Based on previous studies regarding pterosaur ontogeny (Bennett, 1993; Bennett, 1995; Bennett, 1996; Kellner & Tomida, 2000; Kellner et al., 2013; Kellner, 2015), IVPP V 23674 shows evidence of skeletal maturity. Several bones are fused, including the extensor tendon process with the first phalanx of the wing finger, the tibia with the proximal tarsals, and the scapula with the coracoid (Figs. 4D, 4G, 4H). Based on the six ontogenetic stages (OS1–OS6) introduced by Kellner (2015), IVPP V 23674 has reached at least OS5. The holotype of Kunpengopterus sinensis has also several fused bones (Wang et al., 2010), except for the epiphysis with the distal end of the humerus and the proximal tarsal elements with the tibia. Therefore, from the ontogenetic point of view, the holotype (IVPP V 16047) was younger than the new specimen (IVPP V 23674). The maximized wingspan (see Kellner et al., 2013) of IVPP V 23674 is about 790 mm. This is roughly 7% larger than the holotype (Table 1; Wang et al., 2010; Cheng et al., 2017).

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 12/20 Figure 6 Reconstructions of wukongopterid feet with all metatarsals II of the same size. Showing metatarsals II and IV in light grey, first phalanges of pedal digit V in dark grey and second phalanges in black. Scale bars: 10 mm. (A) Wukongopterus (based on Wang et al., 2009). (B) Darwinopterus linglongtaensis (based on Wang et al., 2010). (C) Darwinopterus robustodens (based on Lü et al., 2011a). (D) Holotype of Kunpengopterus sinensis (based on Wang et al., 2010). (E) Kunpengopterus sinensis (IVPP V 23674). (F) IVPP V 18403/ZMNH M8802 (wukongopterid with eggs, based on Lü et al., 2011b; Wang et al., 2015). Full-size DOI: 10.7717/peerj.4102/fig-6

Pterosaur material with a well-preserved palatal region is not common (e.g., Ősi et al., 2010; Kellner, 2013; Zhou et al., 2017), especially considering non-pterodactyloids (Wellnhofer, 1978). Regarding the Wukongopteridae, despite the several specimens described so far, none has the palate exposed (Wang et al., 2009; Wang et al., 2010; Lü et al., 2010; Lü et al., 2011a; Cheng et al., 2016). Based on IVPP V 23674, one of the most remarkable palatal features of Kunpengopterus sinensis is the very large postpalatine fenestra that reaches almost the same length as the choanae (Figs. 2 and 5), what was never observed in any pterosaur before (e.g., Williston, 1902; Wellnhofer, 1978; Wang et al., 2008; Bennett, 2013; Ősi et al., 2010; Pinheiro & Schultz, 2012; Kellner, 2013). The choanae are reduced, smaller and positioned more posteriorly

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 13/20 than the postpalatine fenestrae, which is also observed for the first time in pterosaurs (Figs. 2 and 5). Ősi et al. (2010) reviewed the palate of pterosaurs and pointed out that the lateral process of the pterygoid that divided the subtemporal fenestra in non-pterodactyloids was lost in pterodactyloids, which was challenged by some recent discoveries (e.g., Kellner, 2013; Zhou et al., 2017). The palate of Kunpengopterus (IVPP V 23674) differs remarkably from that of all other pterosaurs and does not conform to the models proposed by Ősi et al. (2010). Although there are indeed three major palatal openings, as in non-pterodactyloids, the postpalatine fenestra (= suborbital fenestra of Ősi et al., 2010) is the largest reported so far in any pterosaur. These openings extend anteriorly surpassing the anterior margin of the choanae. The latter are also very compressed laterally, being even smaller than the postpalatine fenestrae, unlike the condition observed in pterodactyloids and other non- pterodactyloids. The pterygoids also appear to be more united than in non-pterodactyloids, suggesting that the interpterygoid opening, which is not visible in Kunpengopterus (IVPP V 23674), might have been smaller in this genus (or in wukongopterids) than in more basal non-pterodactyloids. This odd morphology indicates that the evolution of the palate in pterosaurs was more complex than previously thought. It is possible that the configuration of the palate observed in IVPP V 23674 might be similar to that of other wukongopterids and therefore could potentially provide several new autapomorphies for this quite remarkable clade. Regarding the sesamoid bones found associated with the manual unguals of Kunpengopterus, such elements were also reported in Darwinopterus linglongtaensis (IVPP V 16049), an individual that lacks the fusion of proximal and distal carpal elements and was therefore ontogenetically less developed (probably OS3 of Kellner, 2015) than the two specimens of this genus. This suggests that ungual sesamoids appear very early in the ontogenetic development of these pterosaurs and might have been widespread among wukongopterids. The fact that they have not been reported so far might be due to overlooking, poor preservation or loss during preparation. The presence of sesamoid bones at the dorsal side of manual unguals have been reported in many basal pterosaurs (e.g., Wild, 1978; Wild, 1994; Padian, 1983; Padian, 2008; Dalla Vecchia, 2009). These ossifications were probably connected with the extensor digitorum brevis (Bennett, 2008), whose function has been linked with grasping capabilities, climbing and terrestrial locomotion (Unwin, 1988; Bennett, 1997; Witton, 2015). The presence of a sesamoid is also observed in at least one pedal phalanx of the holotype (IVPP V 16047) of Kunpengopterus sinensis. Therefore, arboreal behavior for this pterosaur and other wukongopterids is a strong possibility that cannot be ruled out. Regarding the feet of other wukongopterids, Kunpengopterus shows a shorter first phalanx of pedal digit V that is less than 70% the length of metatarsal IV (Table 4). Furthermore, the second pedal phalanx of digit V is bent very close to the proximal end, with both sections forming an angle of around 145◦. Wang et al. (2015) regarded a specimen (IVPP V 18403/ZMNH M8802) as potentially representing Kunpengopterus sp. However, the feet of IVPP V 18403/ZMNH M8802 differ from other wukongopterids by having the first phalanx of pedal digit V longer than

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 14/20 metatarsal IV and the second phalanx of pedal digit V curved at about the middle part of this bone, forming an angle of 137◦ (Table 4). Although the detailed study of this specimen is beyond the scope of this paper, it appears that IVPP V 18403/ZMNH M88 might present a distinct taxon at least at a species level.

CONCLUSION The discovery of a second specimen (IVPP V 23674) of Kunpengopterus sinensis provides new information for this species, including anatomy and ontogeny. IVPP V 23674 can be classified in a later ontogenetic stage (at least OS5) than the holotype. It shows that the fusion of ilium and sacral vertebrae has not been completed at this stage. The new specimen sheds light on the wukongopterid palate that differs from all other pterosaurs by the presence of extremely elongated postpalatine fenestrae that reach anterior to the anterior margin of the choanae, and choanae that are very compressed laterally. This indicates that the palate development in pterosaurs was more complex than previously thought. The present study shows the presence of sesamoid bones at the dorsal side of manual unguals, which are reported for the first time in this non-pterodactyloid clade. Based on the differences between the wukongopterid pes, Kunpengopterus differs from others by showing a shorter first phalanx and the shortest proximal segment of the second phalanx of pedal digit V, indicating that the feet are relevant for wukongopterid taxonomy.

ACKNOWLEDGEMENTS We thank L Xiang (IVPP) for the preparation of the specimen, W Gao (IVPP) for the photos. We acknowledge David Unwin for several suggestions regarding an earlier version of this manuscript.

ADDITIONAL INFORMATION AND DECLARATIONS

Funding This study was supported by the National Natural Science Foundation of China (41572020, 41688103), the Major Research plan of the National Natural Science Foundation of China (91514302), the Strategic Priority Research Program (B) of Chinese Academy of Sciences (XDB18000000), the Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology (CAS), the Hundred Talents Project of Chinese Academy of Sciences, the National Science Fund for Distinguished Young Scholars (40825005), the National Key Basic Research Program of China (2012CB821900), and the Fundacão¸ Cearense de Apoio ao Desenvolvimento Científico e Tecnológico FUNCAP (DCR-0024-02039.01.00/). The Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq, (CNPq # 304780/2013-8) and the Fundacão¸ Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ # E-26/202.893/2015) supported research in China. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 15/20 Grant Disclosures The following grant information was disclosed by the authors: National Natural Science Foundation of China: 41572020, 41688103. Major Research plan of the National Natural Science Foundation of China: 91514302. Chinese Academy of Sciences: XDB18000000. Nanjing Institute of Geology and Palaeontology (CAS). Hundred Talents Project of Chinese Academy of Sciences. National Science Fund for Distinguished Young Scholars: 40825005. National Key Basic Research Program of China: 2012CB821900. Fundacão¸ Cearense de Apoio ao Desenvolvimento Científico e Tecnológico FUNCAP: DCR-0024-02039.01.00/. Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq: CNPq # 304780/2013-8. Fundacão¸ Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro: FAPERJ # E-26/202.893/2015. Competing Interests The authors declare there are no competing interests. Author Contributions • Xin Cheng conceived and designed the experiments, performed the experiments, analyzed the data, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper. • Shunxing Jiang reviewed drafts of the paper. • Xiaolin Wang conceived and designed the experiments, contributed reagents/material- s/analysis tools, reviewed drafts of the paper. • Alexander W.A. Kellner analyzed the data, reviewed drafts of the paper. Data Availability The following information was supplied regarding data availability: The specimen (IVPP V 23674) described in this article is housed at the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences.

REFERENCES Bennett SC. 1993. The ontogeny in Pteranodon and other pterosaurs. Paleobiology 19:92–106 DOI 10.1017/S0094837300012331. Bennett SC. 1995. A statistical study of Rhamphorhynchus from the Solnhofen Limestone of Germany: year-classes of a single large species. Journal of Paleontology 69:569–580 DOI 10.1017/S0022336000034946. Bennett SC. 1996. Year-classes of pterosaurs from the Solnhofen limestones of Germany: taxonomic and systematic implications. Journal of Vertebrate Paleontoloty 16:432–444 DOI 10.1080/02724634.1996.10011332.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 16/20 Bennett SC. 1997. The arboreal leaping theory of the origin of pterosaur flight. Historical Biology 12:265–290 DOI 10.1080/08912969709386566. Bennett SC. 2008. Morphological evolution of the wing of pterosaurs: myology and function. Zitteliana B28:127–141. Bennett SC. 2013. The morphology and taxonomy of the pterosaur Cycnorham- phus. Neues Jahrbuch für Geologie und Paläontologie-Abhandlungen 267:23–41 DOI 10.1127/0077-7749/2012/0295. Cheng X. 2013. Linglongta Pterosaur Fauna and its geological age from Jianchang, western Liaoning, China. DSc thesis, University of Chinese Academy of Sciences [in Chinese with English abstract]. Cheng X, Jiang SX, Wang XL, Kellner AWA. 2016. New information on the Wukon- gopteridae (Pterosauria) revealed by a new specimen from the Jurassic of China. PeerJ 4:e2177 DOI 10.7717/peerj.2177. Cheng X, Jiang SX, Wang XL, Kellner AWA. 2017. Premaxillary crest variation with in the Wukongopteridae (Reptilia, Pterosauria) and comments on cranial structures in pterosaurs. Anais da Academia Brasileira de Ciencias 89:119–130 DOI 10.1590/0001-3765201720160742. Cheng X, Wang XL, Jiang SX, Kellner AWA. 2012. A new scaphognathid pterosaur from western Liaoning, China. Historical Biology 24:101–111 DOI 10.1080/08912963.2011.635423. Cheng X, Wang XL, Jiang SX, Kellner AWA. 2015. Short note on a non-pterodactyloid pterosaur from Upper Jurassic deposits of Inner Mongolia, China. Historical Biology 27:749–754 DOI 10.1080/08912963.2014.974038. Chiappe LM, Kellner AWA, Rivarola D, Davila S, Fox M. 2000. Cranial morphology of Pterodaustro guinazui (Pterosauria: Pterodactyloidea) from the Lower Cretaceous of Argentina. Natural History Museum of Los Angeles County, Contributions in Science 483:1–19. Dalla Vecchia FM. 2009. Anatomy and systematics of the pterosaur Carniadactylus gen. n. Rosenfeldi (Dalla Vecchia, 1995). Rivista Italiana di Paleontologia e stratigrafia 115:159–188. Jiang SX, Cheng X, Ma YX, Wang XL. 2016. A new archaeopterocactyloid pterosaur from the Jiufotang Formation of western Liaoning, China, with a comparison of sterna in Pterodactylomorpha. Journal of Vertebrate Paleontoloty 36:e1212058 DOI 10.1080/02724634.2016.1212058. Jiang SX, Wang XL. 2011. Important features of Gegepterus changae (Pterosauria: Archaeopterodactyloidea, Ctenochasmatidae) from a new specimen. Vertebrata Palasiatica 49:172–184. Jiang SX, Wang XL, Meng X, Cheng X. 2014. A new boreopterid pterosaur from the Lower Cretaceous of western Liaoning, China, with a reassessment of the phylogenetic relationships of the Boreopteridae. Journal of Paleontology 88:823–828 DOI 10.1666/13-068. Kellner AWA. 1994. Remarks on pterosaur taphonomy and paleoecology. Acta Geologica Leopoldensia 39:175–189.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 17/20 Kellner AWA. 2003. Pterosaur phylogeny and comments on the evolutionary history of the group. In: Buffetaut E, Mazin JM, eds. Evolution and palaeonbiology of pterosaurs. London: The Geological Society, 105–137. Kellner AWA. 2013. A new unusual tapejarid (Pterosauria, Pterodactyloidea) from the Early Cretaceous Romualdo Formation, Araripe Basin, Brazil. Earth and Environmental Science Transaction of the Royal Society of Edinburgh 103:409–421 DOI 10.1017/S1755691013000327. Kellner AWA. 2015. Comments on Triassic perosaurs with discussion about ontogeny and description of new taxa. Anais da Academia Brasileira de Ciencias 87:669–689 DOI 10.1590/0001-3765201520150307. Kellner AWA, Campos DA, Sayão JM, Saraiva AAF, Rodrigues T, Oliveira G, Cruz LA, Costa FR, Silva HP, Ferreira JS. 2013. The largest flying reptile from Gondwana: a new specimen of Tropeognathus cf. T. mesembrinus Wellnhofer, 1987 (Pterodacty- loidea, Anhangueridae) and other large pterosaurs from the Romualdo Formation, Lower Cretaceous, Brazil. Anais da Academia Brasileira de Ciencias 85:113–135 DOI 10.1590/S0001-37652013000100009. Kellner AWA, Tomida Y. 2000. Description of a new species of Anhangueridae (Pterodacty- loidea) with comments on the pterosaur fauna from the Santana Formation (Aptian- Albian), Northeastern Brazil. Tokyo: National Science Museum Monographs. Lü JC. 2009. A new non-pterodactyloid pterosaur from Qinglong County, Hebei Province of China. Acta Geologica Sinica English Edition 83:189–199 DOI 10.1111/j.1755-6724.2009.00062.x. Lü JC, Unwin DM, Deeming DC, Jin XS, Liu YQ, Ji Q. 2011b. An egg-adult association, gender, and reproduction in pterosaurs. Science 331:321–324 DOI 10.1126/science.1197323. Lü JC, Unwin DM, Jin XS, Liu YQ, Ji Q. 2010. Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull. Proceedings of the Royal Society B 277:383–389 DOI 10.1098/rspb.2009.1603. Lü JC, Xu L, Chang HL, Zhang XL. 2011a. A new darwinopterid pterosaur from the Mid- dle Jurassic of western Liaoning, northeastern China and its ecological implications. Acta Geologica Sinica English Edition 85:507–514 DOI 10.1111/j.1755-6724.2011.00444.x. Manzig PC, Kellner AWA, Weinschütz LC, Fragoso CE, Vega CS, Guimarães GB, Godoy LC, Liccardo A, Ricetti JH, De Moura CC. 2014. Discovery of a rare pterosaur bone bed in a Cretaceous desert with insights on ontogeny and behavior of flying reptiles. PLOS ONE 9:e100005 DOI 10.1371/journal.pone.0100005. Ősi A, Prondvai E, Frey E, Pohl B. 2010. New interpretation of the palate of pterosaurs. The Anatomical Record 293:243–258 DOI 10.1002/ar.21053. Padian K. 1983. Osteology and functional morphology of Dimorphodon macronyx (Buckland) (Pterosauria: Rhamphorhynchoidea) based on new material in the Yale Peabody Museum. Postilla 189:1–44. Padian K. 2008. The early Jurassic pterosaur Dorygnathus banthensis (Theodori, 1830). Special Papers in Palaeontology 80:1–64.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 18/20 Pinheiro FL, Schultz CL. 2012. An unusual pterosaur specimen (Pterodacty- loidea, ? Azhdarchoidea) from the Early Cretaceous Romualdo Formation of Brazil, and the evolution of the pterodactyloid palate. PLOS ONE 7:e50088 DOI 10.1371/journal.pone.0050088. Rodrigues T, Jiang SX, Cheng X, Wang XL, Kellner AWA. 2015. A new toothed pter- anodontoid (Pterosauria, Pterodactyloidea) from the Jiufotang Formation (Lower Cretaceous, Aptian) of China and comments on Liaoningopterus gui Wang and Zhou, 2003. Historical Biology 27:782–795 DOI 10.1080/08912963.2015.1033417. Sullivan C, Wang Y, Hone DWE, Wang YQ, Xu X, Zhang FC. 2014. The vertebrates of the Jurassic Daohugou Biota of northeastern China. Journal of Vertebrate Paleontol- ogy 34:243–280 DOI 10.1080/02724634.2013.787316. Unwin DM. 1988. New remains of the pterosaur Dimorphodon (Pterosauria: Rham- phorhynchoidea) and the terrestrial ability of early pterosaurs. Modern Geology 13:57–68. Wang XL, Campos DA, Zhou ZH, Kellner AWA. 2008. A primitive istiodactylid pterosaur (Pterodactyloidea) from the Jiufotang Formation (Early Cretaceous), northeast China. Zootaxa 1813:1–18. Wang XL, Cheng X, Jiang SX, Wang Q, Meng X, Zhang JL, Li N. 2014c. Timing of Linglongta Pterosaur Fauna from Western Liaoning and Zhejiangopterus: a summary of geochronology and stratigraphic sequence of pterosaur fossil-bearing beds in China. Earth Science Frontiers 21:157–184 [In Chinese with English abstract]. Wang XL, Kellner AWA, Cheng X, Jiang SX, Wang Q, Sayão JM, Rodrigues T, Costa F, Li N, Meng X, Zhou ZH. 2015. Eggshell and histology provide insight on the life history of a pterosaur with two functional ovaries. Anais da Academia Brasileira de Ciencias 87:1599–1609 DOI 10.1590/0001-3765201520150364. Wang XL, Kellner AWA, Jiang SX, Cheng X. 2012. New toothed flying reptile from Asia: close similarities between early Cretaceous pterosaur faunas from China and Brazil. Naturwissenschaften 99:249–257 DOI 10.1007/s00114-012-0889-1. Wang XL, Kellner AWA, Jiang SX, Cheng X, Meng X, Rodrigues T. 2010. New long- tailed pterosaurs (Wukongopteridae) from western Liaoning, China. Anais da Academia Brasileira de Ciencias 82:1045–1062 DOI 10.1590/S0001-37652010000400024. Wang XL, Kellner AWA, Jiang SX, Meng X. 2009. An unusual long-tailed pterosaur with elongated neck from western Liaoning of China. Anais da Academia Brasileira de Ciencias 81:793–812 DOI 10.1590/S0001-37652009000400016. Wang XL, Kellner AWA, Jiang SX, Wang Q, Ma YX, Paidoula Y, Cheng X, Rodrigues T, Meng X, Zhang JL, Li N, Zhou ZH. 2014a. Sexually dimorphic tridimensionally preserved pterosaurs and their eggs from China. Current Biology 24:1323–1330 DOI 10.1016/j.cub.2014.04.054. Wang XL, Kellner AWA, Zhou ZH, Campos DA. 2007. A new pterosaur (Ctenochas- matidae, Archaeopterodactyloidea) from the Lower Cretaceous Yixian Formation of China. Cretaceous Research 28:245–260 DOI 10.1016/j.cretres.2006.08.004.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 19/20 Wang XL, Rodrigues T, Jiang SX, Cheng X, Kellner AWA. 2014b. An Early Cretaceous pterosaur with an unusual mandibular crest from China and a potential novel feeding strategy. Scientific Reports 4:6329 DOI 10.1038/srep06329. Wellnhofer P. 1978. Pterosauria. Handbuch der Palaeoherpetologie, Teil 19. Stuttgart: Gustav Fischer Verlag, 82. Wellnhofer P. 1991. The illustrated encyclopedia of pterosaurs. London: Salamander books Ltd, 192. Wild R. 1978. Die Flugsaurier (Reptilia, Pterosauria) aus der Oberen Trias von Cene bei Bergamo, Italien. Bolletino della Societa Paleontologica Italiana 17:176–256. Wild R. 1994. A juvenile specimen of Eudimorphodon ranzii Zambelli (Reptilia, Pterosauria) from the Upper Triassic (Norian) of Bergamo. Rivista del Museo Civico di Scienze Naturali ‘‘E. Caffi’’ Bergamo 16:91–115. Williston SW. 1902. On the skull of Nyctodactylus, an Upper Cretaceous pterodactyl. Journal of Geology 10:520–531 DOI 10.1086/621025. Witton MP. 2015. Were early pterosaurs inept terrestrial locomotoers? PeerJ 3:e1018 DOI 10.7717/peerj.1018. Zhou CF, Gao KQ, Yi HY, Xue JZ, Li GQ, Fox RC. 2017. Earliest filter-feeding pterosaur from the Jurassic of China and ecological evolution of Pterodactyloidea. Royal Society Open Science 4:160672 DOI 10.1098/rsos.160672. Zhou ZH, Jin F, Wang Y. 2010. Vertebrate assemblages from the middle-late Jurassic Yanliao Biota in Northeast China. Earth Science Frontiers 17(Special Issue):252–254. Zhou CF, Schoch RP. 2011. New material of the non-pterodactyloid pterosaur Changchengopterus pani (Lü, 2009) from the Late Jurassic Tiaojishan Formation of western Liaoning. Neues Jahrbuch für Geologie und Paläontologie-Abhandlungen 260:265–275 DOI 10.1127/0077-7749/2011/0131.

Cheng et al. (2017), PeerJ, DOI 10.7717/peerj.4102 20/20